The transcriptome landscapes of citrus leaf in different developmental stages.
Asian citrus psyllids
Citrus
Diaphorina citri
Immature leaf
Leaf development
Liberibacter
Mature leaf
Sugars
Xanthomonas citri
Journal
Plant molecular biology
ISSN: 1573-5028
Titre abrégé: Plant Mol Biol
Pays: Netherlands
ID NLM: 9106343
Informations de publication
Date de publication:
Jul 2021
Jul 2021
Historique:
received:
22
01
2021
accepted:
12
04
2021
pubmed:
20
4
2021
medline:
22
7
2021
entrez:
19
4
2021
Statut:
ppublish
Résumé
The temporal expression profiles of citrus leaves explain the sink-source transition of immature leaves to mature leaves and provide knowledge regarding the differential responses of mature and immature leaves to biotic stress such as citrus canker and Asian citrus psyllid (Diaphorina citri). Citrus is an important fruit crop worldwide. Different developmental stages of citrus leaves are associated with distinct features, such as differences in susceptibilities to pathogens and insects, as well as photosynthetic capacity. Here, we investigated the mechanisms underlying these distinctions by comparing the gene expression profiles of mature and immature citrus leaves. Immature (stages V3 and V4), transition (stage V5), and mature (stage V6) Citrus sinensis leaves were chosen for RNA-seq analyses. Carbohydrate biosynthesis, photosynthesis, starch biosynthesis, and disaccharide metabolic processes were enriched among the upregulated differentially expressed genes (DEGs) in the V5 and V6 stages compared with that in the V3 and V4 stages. Glucose level was found to be higher in V5 and V6 than in V3 and V4. Among the four stages, the largest number of DEGs between contiguous stages were identified between V5 and V4, consistent with a change from sink to source, as well as with the sucrose and starch quantification data. The differential expression profiles related to cell wall synthesis, secondary metabolites such as flavonoids and terpenoids, amino acid biosynthesis, and immunity between immature and mature leaves may contribute to their different responses to Asian citrus psyllid infestation. The expression data suggested that both the constitutive and induced gene expression of immunity-related genes plays important roles in the greater resistance of mature leaves against Xanthomonas citri compared with immature leaves. The gene expression profiles in the different stages can help identify stage-specific promoters for the manipulation of the expression of citrus traits according to the stage. The temporal expression profiles explain the sink-source transition of immature leaves to mature leaves and provide knowledge regarding the differential responses to biotic stress.
Identifiants
pubmed: 33871796
doi: 10.1007/s11103-021-01154-8
pii: 10.1007/s11103-021-01154-8
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
349-366Informations de copyright
© 2021. The Author(s), under exclusive licence to Springer Nature B.V.
Références
Albert LP, Wu J, Prohaska N, de Camargo PB, Huxman TE, Tribuzy ES, Ivanov VY, Oliveira RS, Garcia S, Smith MN, Oliveira Junior RC, Restrepo-Coupe N, da Silva R, Stark SC, Martins GA, Penha DV, Saleska SR (2018) Age-dependent leaf physiology and consequences for crown-scale carbon uptake during the dry season in an Amazon evergreen forest. New Phytol 219(3):870–884. https://doi.org/10.1111/nph.15056
doi: 10.1111/nph.15056
pubmed: 29502356
An SQ, Potnis N, Dow M, Vorhölter FJ, He YQ, Becker A, Teper D, Li Y, Wang N, Bleris L, Tang JL (2020) Mechanistic insights into host adaptation, virulence and epidemiology of the phytopathogen Xanthomonas. FEMS Microbiol Rev 44(1):1–32. https://doi.org/10.1093/femsre/fuz024
doi: 10.1093/femsre/fuz024
pubmed: 31578554
Anders S, Pyl PT, Huber W (2015) HTSeq–a Python framework to work with high-throughput sequencing data. Bioinformatics 31(2):166–169. https://doi.org/10.1093/bioinformatics/btu638
doi: 10.1093/bioinformatics/btu638
Azam M, Jiang Q, Zhang B, Xu C, Chen K (2013) Citrus leaf volatiles as affected by developmental stage and genetic type. Int J Mol Sci 14(9):17744–17766. https://doi.org/10.3390/ijms140917744
doi: 10.3390/ijms140917744
pubmed: 23994837
pmcid: 3794751
Balagué C, Gouget A, Bouchez O, Souriac C, Haget N, Boutet-Mercey S, Govers F, Roby D, Canut H (2017) The Arabidopsis thaliana lectin receptor kinase LecRK-I.9 is required for full resistance to Pseudomonas syringae and affects jasmonate signalling. Mol Plant Pathol 18(7):937–948. https://doi.org/10.1111/mpp.12457
doi: 10.1111/mpp.12457
pubmed: 27399963
Beck M, Wyrsch I, Strutt J, Wimalasekera R, Webb A, Boller T, Robatzek S (2014) Expression patterns of flagellin sensing 2 map to bacterial entry sites in plant shoots and roots. J Exp Bot 65(22):6487–6498. https://doi.org/10.1093/jxb/eru366
doi: 10.1093/jxb/eru366
pubmed: 25205577
pmcid: 4246182
Bent AF, Kunkel BN, Dahlbeck D, Brown KL, Schmidt R, Giraudat J, Leung J, Staskawicz BJ (1994) RPS2 of Arabidopsis thaliana: a leucine-rich repeat class of plant disease resistance genes. Science 265(5180):1856–1860. https://doi.org/10.1126/science.8091210
doi: 10.1126/science.8091210
pubmed: 8091210
Bonnot T, Gillard MB, Nagel DH (2019) A simple protocol for informative visualization of enriched gene ontology terms. Bio-Protoc 9(22):e3429. https://doi.org/10.21769/BioProtoc.3429
doi: 10.21769/BioProtoc.3429
Bouhassan A, Sadiki M, Tivoli B, Porta-Puglia A (2004) Influence of growth stage and leaf age on expression of the components of partial resistance of faba bean to Botrytis fabae Sard. Phytopathol Mediterran. https://doi.org/10.14601/Phytopathol_Mediterr-1768
doi: 10.14601/Phytopathol_Mediterr-1768
Bové JM (2006) Huanglongbing: a destructive, newly-emerging, century-old disease of citrus. J Plant Pathol 88:7–37
Cechin I, Corniani N, Fumis TdF, Cataneo AC (2010) Differential responses between mature and young leaves of sunflower plants to oxidative stress caused by water deficit. Ciência Rural 40:1290–1294
doi: 10.1590/S0103-84782010000600008
Cernadas RA, Benedetti CE (2009) Role of auxin and gibberellin in citrus canker development and in the transcriptional control of cell-wall remodeling genes modulated by Xanthomonas axonopodis pv. citri. Plant Sci 177(3):190–195. https://doi.org/10.1016/j.plantsci.2009.05.006
doi: 10.1016/j.plantsci.2009.05.006
Chan W-K, Tan LT, Chan K-G, Lee L-H, Goh B-H (2016) Nerolidol: a sesquiterpene alcohol with multi-faceted pharmacological and biological activities. Molecules. https://doi.org/10.3390/molecules21050529
doi: 10.3390/molecules21050529
pubmed: 27618002
pmcid: 6273902
Cifuentes-Arenas JC, de Goes A, de Miranda MP, Beattie GAC, Lopes SA (2018) Citrus flush shoot ontogeny modulates biotic potential of Diaphorina citri. PLoS ONE 13(1):e0190563. https://doi.org/10.1371/journal.pone.0190563
doi: 10.1371/journal.pone.0190563
pubmed: 29304052
pmcid: 5755881
Coleman JS (1986) Leaf development and leaf stress: increased susceptibility associated with sink-source transition. Tree Physiol 2:289–299. https://doi.org/10.1093/treephys/2.1-2-3.289
doi: 10.1093/treephys/2.1-2-3.289
pubmed: 14975862
Datta K, Vasquez A, Tu J, Torrizo L, Alam MF, Oliva N, Abrigo E, Khush GS, Datta SK (1998) Constitutive and tissue-specific differential expression of the cryIA(b) gene in transgenic rice plants conferring resistance to rice insect pest. Theor Appl Genet 97(1):20–30. https://doi.org/10.1007/s001220050862
doi: 10.1007/s001220050862
Daudet FA, Lacointe A, Gaudillère JP, Cruiziat P (2002) Generalized Münch coupling between sugar and water fluxes for modelling carbon allocation as affected by water status. J Theor Biol 214(3):481–498. https://doi.org/10.1006/jtbi.2001.2473
doi: 10.1006/jtbi.2001.2473
pubmed: 11846604
Duan S, Jia H, Pang Z, Teper D, White F, Jones J, Zhou C, Wang N (2018) Functional characterization of the citrus canker susceptibility gene CsLOB1. Mol Plant Pathol 19(8):1908–1916. https://doi.org/10.1111/mpp.12667
doi: 10.1111/mpp.12667
pmcid: 6638005
Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185–209. https://doi.org/10.1146/annurev.phyto.42.040803.140421
doi: 10.1146/annurev.phyto.42.040803.140421
pubmed: 15283665
Fancelli M, Borges M, Laumann RA, Pickett JA, Birkett MA, Blassioli-Moraes MC (2018) Attractiveness of host plant volatile extracts to the Asian Citrus Psyllid, Diaphorina citri, is reduced by Terpenoids from the non-host cashew. J Chem Ecol 44(4):397–405. https://doi.org/10.1007/s10886-018-0937-1
doi: 10.1007/s10886-018-0937-1
pubmed: 29500752
pmcid: 5899996
Ference CM, Gochez AM, Behlau F, Wang N, Graham JH, Jones JB (2018) Recent advances in the understanding of Xanthomonas citri ssp. citri pathogenesis and citrus canker disease management. Mol Plant Pathol 19(6):1302–1318. https://doi.org/10.1111/mpp.12638
doi: 10.1111/mpp.12638
pubmed: 29105297
pmcid: 6638175
Franco JY, Thapa SP, Pang Z, Gurung FB, Liebrand TWH, Stevens DM, Ancona V, Wang N, Coaker G (2020) Citrus Vascular Proteomics highlights the role of peroxidases and serine proteases during Huanglongbing disease progression. Mol Cell Proteomics 19(12):1936–1952. https://doi.org/10.1074/mcp.RA120.002075
doi: 10.1074/mcp.RA120.002075
pubmed: 32883801
Ge SX, Son EW, Yao R (2018) iDEP: an integrated web application for differential expression and pathway analysis of RNA-Seq data. BMC Bioinformatics 19(1):534. https://doi.org/10.1186/s12859-018-2486-6
doi: 10.1186/s12859-018-2486-6
pubmed: 30567491
pmcid: 6299935
Grafton-Cardwell EE, Stelinski LL, Stansly PA (2013) Biology and management of Asian citrus psyllid, vector of the huanglongbing pathogens. Annu Rev Entomol 58:413–432. https://doi.org/10.1146/annurev-ento-120811-153542
doi: 10.1146/annurev-ento-120811-153542
pubmed: 23317046
Graham JH, Gottwald TR, Cubero J, Achor DS (2004) Xanthomonas axonopodis pv. citri: factors affecting successful eradication of citrus canker. Mol Plant Pathol 5(1):1–15. https://doi.org/10.1046/j.1364-3703.2004.00197.x
doi: 10.1046/j.1364-3703.2004.00197.x
pubmed: 20565577
Grant MR, Godiard L, Straube E, Ashfield T, Lewald J, Sattler A, Innes RW, Dangl JL (1995) Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance. Science 269(5225):843–846. https://doi.org/10.1126/science.7638602
doi: 10.1126/science.7638602
pubmed: 7638602
Hall DG, Albrecht U, Bowman KD (2016) Transmission rates of ‘Ca. Liberibacter asiaticus’ by Asian Citrus Psyllid are enhanced by the presence and developmental stage of citrus flush. J Econ Entomol 109(2):558–563. https://doi.org/10.1093/jee/tow009
doi: 10.1093/jee/tow009
pubmed: 26884596
Hall DG, Sétamou M, Mizell RF (2010) A comparison of sticky traps for monitoring Asian citrus psyllid (Diaphorina citri Kuwayama). Crop Prot 29(11):1341–1346. https://doi.org/10.1016/j.cropro.2010.06.003
doi: 10.1016/j.cropro.2010.06.003
Hildebrandt Tatjana M, Nunes Nesi A, Araújo Wagner L, Braun H-P (2015) Amino acid catabolism in plants. Mol Plant 8(11):1563–1579. https://doi.org/10.1016/j.molp.2015.09.005
doi: 10.1016/j.molp.2015.09.005
pubmed: 26384576
Huang X, Wang Y, Xu J, Wang N (2020) Development of multiplex genome editing toolkits for citrus with high efficacy in biallelic and homozygous mutations. Plant Mol Biol 104(3):297–307. https://doi.org/10.1007/s11103-020-01043-6
doi: 10.1007/s11103-020-01043-6
pubmed: 32748081
Jager CE, Symons GM, Glancy NE, Reid JB, Ross JJ (2007) Evidence that the mature leaves contribute auxin to the immature tissues of pea (Pisum sativum L.). Planta 226(2):361–368. https://doi.org/10.1007/s00425-007-0487-1
doi: 10.1007/s00425-007-0487-1
pubmed: 17308928
Jalan N, Kumar D, Andrade MO, Yu F, Jones JB, Graham JH, White FF, Setubal JC, Wang N (2013) Comparative genomic and transcriptome analyses of pathotypes of Xanthomonas citri subsp. citri provide insights into mechanisms of bacterial virulence and host range. BMC Genomics 14:551. https://doi.org/10.1186/1471-2164-14-551
doi: 10.1186/1471-2164-14-551
pubmed: 23941402
pmcid: 3751643
Jashni MK, Mehrabi R, Collemare J, Mesarich CH, de Wit PJGM (2015) The battle in the apoplast: further insights into the roles of proteases and their inhibitors in plant-pathogen interactions. Front Plant Sci 6:584–584. https://doi.org/10.3389/fpls.2015.00584
doi: 10.3389/fpls.2015.00584
pubmed: 26284100
pmcid: 4522555
Jia H, Orbović V, Wang N (2019) CRISPR-LbCas12a-mediated modification of citrus. Plant Biotechnol J. https://doi.org/10.1111/pbi.13109
doi: 10.1111/pbi.13109
pubmed: 31199554
pmcid: 6920336
Jia H, Wang N (2014a) Targeted genome editing of sweet orange using Cas9/sgRNA. PLoS ONE 9(4):e93806. https://doi.org/10.1371/journal.pone.0093806
doi: 10.1371/journal.pone.0093806
pubmed: 24710347
pmcid: 3977896
Jia H, Wang N (2014b) Xcc-facilitated agroinfiltration of citrus leaves: a tool for rapid functional analysis of transgenes in citrus leaves. Plant Cell Rep 33(12):1993–2001. https://doi.org/10.1007/s00299-014-1673-9
doi: 10.1007/s00299-014-1673-9
pubmed: 25146436
Jia H, Wang N (2020) Generation of homozygous canker-resistant citrus in the T0 generation using CRISPR-SpCas9p. Plant Biotechnol J. https://doi.org/10.1111/pbi.13375
doi: 10.1111/pbi.13375
pubmed: 32167662
pmcid: 7540605
Jia H, Xu J, Orbović V, Zhang Y, Wang N (2017a) Editing citrus genome via SaCas9/sgRNA system. Front Plant Sci 8:2135. https://doi.org/10.3389/fpls.2017.02135
doi: 10.3389/fpls.2017.02135
pubmed: 29312390
pmcid: 5732962
Jia H, Zhang Y, Orbović V, Xu J, White FF, Jones JB, Wang N (2017b) Genome editing of the disease susceptibility gene CsLOB1 in citrus confers resistance to citrus canker. Plant Biotechnol J 15(7):817–823. https://doi.org/10.1111/pbi.12677
doi: 10.1111/pbi.12677
pubmed: 27936512
pmcid: 5466436
Kaloshian I, Walling LL (2005) Hemipterans as plant pathogens. Annu Rev Phytopathol 43:491–521. https://doi.org/10.1146/annurev.phyto.43.040204.135944
doi: 10.1146/annurev.phyto.43.040204.135944
pubmed: 16078893
Kalve S, De Vos D, Beemster GTS (2014) Leaf development: a cellular perspective. Front Plant Sci 5:362
doi: 10.3389/fpls.2014.00362
Kim D, Paggi JM, Park C, Bennett C, Salzberg SL (2019) Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nat Biotechnol 37(8):907–915. https://doi.org/10.1038/s41587-019-0201-4
doi: 10.1038/s41587-019-0201-4
pubmed: 31375807
pmcid: 7605509
Knoblauch M, Peters WS (2017) What actually is the Münch hypothesis? A short history of assimilate transport by mass flow. J Integr Plant Biol 59(5):292–310. https://doi.org/10.1111/jipb.12532
doi: 10.1111/jipb.12532
pubmed: 28276639
Koch KE (1984) The path of photosynthate translocation into citrus fruit. Plant, Cell Environ 7(9):647–653. https://doi.org/10.1111/1365-3040.ep11571540
doi: 10.1111/1365-3040.ep11571540
Koch M, Mew T (1991) Rate of lesion expansion in leaves as a parameter of resistance to Xanthomonas campestris pv. oryzae in rice. Plant Dis 75:897–900
doi: 10.1094/PD-75-0897
Kolukisaoglu U, Weinl S, Blazevic D, Batistic O, Kudla J (2004) Calcium sensors and their interacting protein kinases: genomics of the Arabidopsis and rice CBL-CIPK signaling networks. Plant Physiol 134(1):43–58. https://doi.org/10.1104/pp.103.033068
doi: 10.1104/pp.103.033068
pubmed: 14730064
pmcid: 316286
Kursar TA, Dexter KG, Lokvam J, Pennington RT, Richardson JE, Weber MG, Murakami ET, Drake C, McGregor R, Coley PD (2009) The evolution of antiherbivore defenses and their contribution to species coexistence in the tropical tree genus Inga. Proc Natl Acad Sci U S A 106(43):18073–18078. https://doi.org/10.1073/pnas.0904786106
doi: 10.1073/pnas.0904786106
pubmed: 19805183
pmcid: 2775284
Kurt S, Tok FM (2006) Influence of inoculum concentration, leaf age, temperature, and duration of leaf wetness on Septoria blight of parsley. Crop Prot 25(6):556–561. https://doi.org/10.1016/j.cropro.2005.08.012
doi: 10.1016/j.cropro.2005.08.012
LeBlanc C, Zhang F, Mendez J, Lozano Y, Chatpar K, Irish VF, Jacob Y (2018) Increased efficiency of targeted mutagenesis by CRISPR/Cas9 in plants using heat stress. Plant J 93(2):377–386. https://doi.org/10.1111/tpj.13782
doi: 10.1111/tpj.13782
pubmed: 29161464
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25(16):2078–2079. https://doi.org/10.1093/bioinformatics/btp352
doi: 10.1093/bioinformatics/btp352
pubmed: 19505943
pmcid: 2723002
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25(4):402–408. https://doi.org/10.1006/meth.2001.1262
doi: 10.1006/meth.2001.1262
pubmed: 11846609
pmcid: 11846609
Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15(12):550. https://doi.org/10.1186/s13059-014-0550-8
doi: 10.1186/s13059-014-0550-8
pubmed: 25516281
pmcid: 25516281
MacRae JC, Smith D, McCready RM (1974) Starch estimation in leaf tissue–a comparison of results using six methods. J Sci Food Agric 25(12):1465–1469. https://doi.org/10.1002/jsfa.2740251206
doi: 10.1002/jsfa.2740251206
pubmed: 4373616
Maness N (2010) Extraction and analysis of soluble carbohydrates. Methods Mol Biol 639:341–370. https://doi.org/10.1007/978-1-60761-702-0_22
doi: 10.1007/978-1-60761-702-0_22
pubmed: 20387058
McCleary BV, Charmier LMJ, McKie VA (2019) Measurement of starch: critical evaluation of current methodology. Starch - Stärke 71(1–2):1800146. https://doi.org/10.1002/star.201800146
doi: 10.1002/star.201800146
McLean FT (1921) A study of the structure of the stomata of two species of citrus in relation to citrus canker. Bull Torrey Bot Club 48(4):101–106. https://doi.org/10.2307/2480340
doi: 10.2307/2480340
Milligan SB, Bodeau J, Yaghoobi J, Kaloshian I, Zabel P, Williamson VM (1998) The root knot nematode resistance gene Mi from tomato is a member of the leucine zipper, nucleotide binding, leucine-rich repeat family of plant genes. Plant Cell 10(8):1307–1319. https://doi.org/10.1105/tpc.10.8.1307
doi: 10.1105/tpc.10.8.1307
pubmed: 9707531
pmcid: 144378
Mindrinos M, Katagiri F, Yu GL, Ausubel FM (1994) The A. thaliana disease resistance gene RPS2 encodes a protein containing a nucleotide-binding site and leucine-rich repeats. Cell 78(6):1089–1099. https://doi.org/10.1016/0092-8674(94)90282-8
doi: 10.1016/0092-8674(94)90282-8
pubmed: 7923358
Misas-Villamil JC, van der Hoorn RAL, Doehlemann G (2016) Papain-like cysteine proteases as hubs in plant immunity. New Phytol 212(4):902–907. https://doi.org/10.1111/nph.14117
doi: 10.1111/nph.14117
pubmed: 27488095
Molla KA, Karmakar S, Chanda PK, Sarkar SN, Datta SK, Datta K (2016) Tissue-specific expression of Arabidopsis NPR1 gene in rice for sheath blight resistance without compromising phenotypic cost. Plant Sci 250:105–114. https://doi.org/10.1016/j.plantsci.2016.06.005
doi: 10.1016/j.plantsci.2016.06.005
pubmed: 27457988
Nakano M, Nishihara M, Yoshioka H, Ohnishi K, Hikichi Y, Kiba A (2014) Silencing of DS2 aminoacylase-like genes confirms basal resistance to Phytophthora infestans in Nicotiana benthamiana. Plant Signal Behav 9(2):e28004–e28004. https://doi.org/10.4161/psb.28004
doi: 10.4161/psb.28004
pubmed: 24514749
pmcid: 4091584
Nikolov LA, Runions A, Das Gupta M, Tsiantis M (2019) Leaf development and evolution. Curr Top Dev Biol 131:109–139. https://doi.org/10.1016/bs.ctdb.2018.11.006
doi: 10.1016/bs.ctdb.2018.11.006
pubmed: 30612614
Pandey SS, Vasconcelos FNC, Wang N (2020) Spatiotemporal dynamics of Candidatus Liberibacter asiaticus colonization inside citrus plant and Huanglongbing disease development. Phytopathology. https://doi.org/10.1094/phyto-09-20-0407-r
doi: 10.1094/phyto-09-20-0407-r
pubmed: 33174821
Patané JSL, Martins J, Rangel LT, Belasque J, Digiampietri LA, Facincani AP, Ferreira RM, Jaciani FJ, Zhang Y, Varani AM, Almeida NF, Wang N, Ferro JA, Moreira LM, Setubal JC (2019) Origin and diversification of Xanthomonas citri subsp. citri pathotypes revealed by inclusive phylogenomic, dating, and biogeographic analyses. BMC Genomics 20(1):700. https://doi.org/10.1186/s12864-019-6007-4
doi: 10.1186/s12864-019-6007-4
pubmed: 31500575
pmcid: 6734499
Peeters PJ, Sanson G, Read J (2007) Leaf biomechanical properties and the densities of herbivorous insect guilds. Funct Ecol 21(2):246–255. https://doi.org/10.1111/j.1365-2435.2006.01223.x
doi: 10.1111/j.1365-2435.2006.01223.x
Pelz-Stelinski KS, Brlansky RH, Ebert TA, Rogers ME (2010) Transmission parameters for Candidatus liberibacter asiaticus by Asian citrus psyllid (Hemiptera: Psyllidae). J Econ Entomol 103(5):1531–1541
doi: 10.1603/EC10123
Pettigrew WT, Vaughn KC (1998) Physiological, structural, and immunological characterization of leaf and chloroplast development in cotton. Protoplasma 202(1):23–37. https://doi.org/10.1007/BF01280872
doi: 10.1007/BF01280872
Reich PB, Walters MB, Ellsworth DS (1992) Leaf life-span in relation to leaf, plant, and stand characteristics among diverse ecosystems. Ecol Monogr 62(3):365–392. https://doi.org/10.2307/2937116
doi: 10.2307/2937116
Robert T (2006) Phloem loading: how leaves gain their independence. Bioscience 56(1):15–24. https://doi.org/10.1641/0006-3568(2006)056[0015:PLHLGT]2.0.CO;2
doi: 10.1641/0006-3568(2006)056[0015:PLHLGT]2.0.CO;2
Rossi M, Goggin FL, Milligan SB, Kaloshian I, Ullman DE, Williamson VM (1998) The nematode resistance gene Mi of tomato confers resistance against the potato aphid. Proc Natl Acad Sci U S A 95(17):9750–9754. https://doi.org/10.1073/pnas.95.17.9750
doi: 10.1073/pnas.95.17.9750
pubmed: 9707547
pmcid: 21408
Saijo Y, Loo EP, Yasuda S (2018) Pattern recognition receptors and signaling in plant-microbe interactions. Plant J 93(4):592–613. https://doi.org/10.1111/tpj.13808
doi: 10.1111/tpj.13808
pubmed: 29266555
Shi Q, Febres VJ, Jones JB, Moore GA (2016) A survey of FLS2 genes from multiple citrus species identifies candidates for enhancing disease resistance to Xanthomonas citri ssp. citri. Hortic Res 3:16022. https://doi.org/10.1038/hortres.2016.22
doi: 10.1038/hortres.2016.22
pubmed: 27222722
pmcid: 4863249
Simmonds MSJ (2001) Importance of flavonoids in insect–plant interactions: feeding and oviposition. Phytochemistry 56(3):245–252. https://doi.org/10.1016/S0031-9422(00)00453-2
doi: 10.1016/S0031-9422(00)00453-2
pubmed: 11243451
Staswick PE, Serban B, Rowe M, Tiryaki I, Maldonado MT, Maldonado MC, Suza W (2005) Characterization of an Arabidopsis enzyme family that conjugates amino acids to indole-3-acetic acid. Plant Cell 17(2):616. https://doi.org/10.1105/tpc.104.026690
doi: 10.1105/tpc.104.026690
pubmed: 15659623
pmcid: 548830
Supek F, Bošnjak M, Škunca N, Šmuc T (2011) REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS ONE 6(7):e21800. https://doi.org/10.1371/journal.pone.0021800
doi: 10.1371/journal.pone.0021800
pubmed: 21789182
pmcid: 3138752
Sétamou M, Alabi OJ, Kunta M, Jifon JL, da Graça JV (2016a) Enhanced acquisition rates of “Candidatus Liberibacter asiaticus” by the Asian Citrus Psyllid (Hemiptera: Liviidae) in the presence of vegetative flush growth in citrus. J Econ Entomol 109(5):1973–1978. https://doi.org/10.1093/jee/tow171
doi: 10.1093/jee/tow171
pubmed: 27451998
Sétamou M, Alabi OJ, Simpson CR, Jifon JL (2017) Contrasting amino acid profiles among permissive and non-permissive hosts of Candidatus Liberibacter asiaticus, putative causal agent of Huanglongbing. PLoS ONE 12(12):e0187921. https://doi.org/10.1371/journal.pone.0187921
doi: 10.1371/journal.pone.0187921
pubmed: 29236706
pmcid: 5728503
Sétamou M, Sanchez A, Saldaña RR, Patt JM, Summy R (2014) Visual responses of adult Asian Citrus Psyllid (Hemiptera: Liviidae) to colored sticky traps on citrus trees. J Insect Behav 27(4):540–553. https://doi.org/10.1007/s10905-014-9448-2
doi: 10.1007/s10905-014-9448-2
Sétamou M, Simpson CR, Alabi OJ, Nelson SD, Telagamsetty S, Jifon JL (2016b) Quality matters: influences of citrus flush physicochemical characteristics on population dynamics of the Asian Citrus Psyllid (Hemiptera: Liviidae). PLoS ONE 11(12):e0168997. https://doi.org/10.1371/journal.pone.0168997
doi: 10.1371/journal.pone.0168997
pubmed: 28030637
pmcid: 5193449
Teper D, Xu J, Li J, Wang N (2020) The immunity of Meiwa kumquat against Xanthomonas citri is associated with a known susceptibility gene induced by a transcription activator-like effector. PLoS Pathog 16(9):e1008886. https://doi.org/10.1371/journal.ppat.1008886
doi: 10.1371/journal.ppat.1008886
pubmed: 32931525
pmcid: 7518600
Tholl D (2015) Biosynthesis and biological functions of terpenoids in plants. Adv Biochem Eng Biotechnol 148:63–106. https://doi.org/10.1007/10_2014_295
doi: 10.1007/10_2014_295
pubmed: 25583224
Tian T, Liu Y, Yan H, You Q, Yi X, Du Z, Xu W, Su Z (2017) agriGO v20: a GO analysis toolkit for the agricultural community, 207 update. Nucleic Acids Res 45(W1):W122-w129. https://doi.org/10.1093/nar/gkx382
doi: 10.1093/nar/gkx382
pubmed: 28472432
pmcid: 5793732
Tomaseto A, Krugner R, Lopes J (2016) Effect of plant barriers and citrus leaf age on dispersal 639 of Diaphorina citri (Hemiptera: Liviidae). J Appl Entomol 140:91–102
doi: 10.1111/jen.12249
Turgeon R (2006) Phloem loading: how leaves gain their independence. Bioscience 56(1):15–24. https://doi.org/10.1641/0006-3568(2006)056[0015:PLHLGT]2.0.CO;2
doi: 10.1641/0006-3568(2006)056[0015:PLHLGT]2.0.CO;2
Vernière CJ, Gottwald TR, Pruvost O (2003) Disease development and symptom expression of Xanthomonas axonopodis pv. citri in various citrus plant tissues. Phytopathology 93(7):832–843. https://doi.org/10.1094/PHYTO.2003.93.7.832
doi: 10.1094/PHYTO.2003.93.7.832
pubmed: 18943164
Vickers CE, Gershenzon J, Lerdau MT, Loreto F (2009) A unified mechanism of action for volatile isoprenoids in plant abiotic stress. Nat Chem Biol 5(5):283–291. https://doi.org/10.1038/nchembio.158
doi: 10.1038/nchembio.158
pubmed: 19377454
Wang N (2019) The citrus Huanglongbing crisis and potential solutions. Mol Plant 12(5):607–609. https://doi.org/10.1016/j.molp.2019.03.008
doi: 10.1016/j.molp.2019.03.008
pubmed: 30947021
Wang N, Pierson EA, Setubal JC, Xu J, Levy JG, Zhang Y, Li J, Rangel LT, Martins J (2017a) The Candidatus liberibacter-host interface: Insights into pathogenesis mechanisms and disease control. Annu Rev Phytopathol. https://doi.org/10.1146/annurev-phyto-080516-035513
doi: 10.1146/annurev-phyto-080516-035513
pubmed: 28637377
Wang N, Stelinski LL, Pelz-Stelinski KS, Graham JH, Zhang Y (2017b) Tale of the Huanglongbing disease pyramid in the context of the citrus microbiome. Phytopathology 107(4):380–387. https://doi.org/10.1094/PHYTO-12-16-0426-RVW
doi: 10.1094/PHYTO-12-16-0426-RVW
pubmed: 28095208
Wang Y, Cordewener JH, America AH, Shan W, Bouwmeester K, Govers F (2015) Arabidopsis lectin receptor kinases LecRK-IX1 and LecRK-IX2 are functional analogs in regulating phytophthora resistance and plant cell death. Mol Plant Microbe Interact 28(9):1032–1048. https://doi.org/10.1094/mpmi-02-15-0025-r
doi: 10.1094/mpmi-02-15-0025-r
pubmed: 26011556
Webber BL, Woodrow IE (2008) Intra-plant variation in cyanogenesis and the continuum of foliar plant defense traits in the rainforest tree Ryparosa kurrangii (Achariaceae). Tree Physiol 28(6):977–984. https://doi.org/10.1093/treephys/28.6.977
doi: 10.1093/treephys/28.6.977
pubmed: 18381278
Wenninger E, Hall D (2007) Daily timing of mating and age at reproductive maturity in Diaphorina citri (Hemiptera : Psyllidae). Florida Entomol 90(4):715–722
doi: 10.1653/0015-4040(2007)90[715:DTOMAA]2.0.CO;2
Won C, Shen X, Mashiguchi K, Zheng Z, Dai X, Cheng Y, Kasahara H, Kamiya Y, Chory J, Zhao Y (2011) Conversion of tryptophan to indole-3-acetic acid by tryptophan aminotransferases of Arabidopsis and YUCCAs in Arabidopsis. Proc Natl Acad Sci 108(45):18518. https://doi.org/10.1073/pnas.1108436108
doi: 10.1073/pnas.1108436108
pubmed: 22025721
pmcid: 3215067
Wroblewski T, Piskurewicz U, Tomczak A, Ochoa O, Michelmore RW (2007) Silencing of the major family of NBS-LRR-encoding genes in lettuce results in the loss of multiple resistance specificities. Plant J 51(5):803–818. https://doi.org/10.1111/j.1365-313X.2007.03182.x
doi: 10.1111/j.1365-313X.2007.03182.x
pubmed: 17587302
Wu GA, Prochnik S, Jenkins J, Salse J, Hellsten U, Murat F, Perrier X, Ruiz M, Scalabrin S, Terol J, Takita MA, Labadie K, Poulain J, Couloux A, Jabbari K, Cattonaro F, Del Fabbro C, Pinosio S, Zuccolo A, Chapman J, Grimwood J, Tadeo FR, Estornell LH, Muñoz-Sanz JV, Ibanez V, Herrero-Ortega A, Aleza P, Pérez-Pérez J, Ramón D, Brunel D, Luro F, Chen C, Farmerie WG, Desany B, Kodira C, Mohiuddin M, Harkins T, Fredrikson K, Burns P, Lomsadze A, Borodovsky M, Reforgiato G, Freitas-Astúa J, Quetier F, Navarro L, Roose M, Wincker P, Schmutz J, Morgante M, Machado MA, Talon M, Jaillon O, Ollitrault P, Gmitter F, Rokhsar D (2014) Sequencing of diverse mandarin, pummelo and orange genomes reveals complex history of admixture during citrus domestication. Nat Biotechnol 32(7):656–662. https://doi.org/10.1038/nbt.2906
doi: 10.1038/nbt.2906
pubmed: 24908277
pmcid: 4113729
Wu GA, Terol J, Ibanez V, López-García A, Pérez-Román E, Borredá C, Domingo C, Tadeo FR, Carbonell-Caballero J, Alonso R, Curk F, Du D, Ollitrault P, Roose ML, Dopazo J, Gmitter FG, Rokhsar DS, Talon M (2018) Genomics of the origin and evolution of citrus. Nature 554(7692):311–316. https://doi.org/10.1038/nature25447
doi: 10.1038/nature25447
pubmed: 29414943
Xu Q, Chen LL, Ruan X, Chen D, Zhu A, Chen C, Bertrand D, Jiao WB, Hao BH, Lyon MP, Chen J, Gao S, Xing F, Lan H, Chang JW, Ge X, Lei Y, Hu Q, Miao Y, Wang L, Xiao S, Biswas MK, Zeng W, Guo F, Cao H, Yang X, Xu XW, Cheng YJ, Xu J, Liu JH, Luo OJ, Tang Z, Guo WW, Kuang H, Zhang HY, Roose ML, Nagarajan N, Deng XX, Ruan Y (2013) The draft genome of sweet orange (Citrus sinensis). Nat Genet 45(1):59–66. https://doi.org/10.1038/ng.2472
doi: 10.1038/ng.2472
pubmed: 23179022
Yan Q, Hu X, Wang N (2012) The novel virulence-related gene nlxA in the lipopolysaccharide cluster of Xanthomonas citri ssp. citri is involved in the production of lipopolysaccharide and extracellular polysaccharide, motility, biofilm formation and stress resistance. Mol Plant Pathol 13(8):923–934. https://doi.org/10.1111/j.1364-3703.2012.00800.x
doi: 10.1111/j.1364-3703.2012.00800.x
pubmed: 22458688
pmcid: 6638664
Yoshimura S, Yamanouchi U, Katayose Y, Toki S, Wang ZX, Kono I, Kurata N, Yano M, Iwata N, Sasaki T (1998) Expression of Xa1, a bacterial blight-resistance gene in rice, is induced by bacterial inoculation. Proc Natl Acad Sci U S A 95(4):1663–1668
doi: 10.1073/pnas.95.4.1663
Zhang J, Huguet-Tapia JC, Hu Y, Jones J, Wang N, Liu S, White FF (2017) Homologues of CsLOB1 in citrus function as disease susceptibility genes in citrus canker. Mol Plant Pathol 18(6):798–810. https://doi.org/10.1111/mpp.12441
doi: 10.1111/mpp.12441
pubmed: 27276658
Zhang Y, Barthe G, Grosser J, Wang N (2016) Transcriptome analysis of root response to citrus blight based on the newly assembled Swingle citrumelo draft genome. BMC Genomics Accepted
Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JD, Felix G, Boller T (2004) Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428(6984):764–767. https://doi.org/10.1038/nature02485
doi: 10.1038/nature02485
pubmed: 15085136
Zou X, Long J, Zhao K, Peng A, Chen M, Long Q, He Y, Chen S (2019) Overexpressing GH3.1 and GH3.1L reduces susceptibility to Xanthomonas citri subsp. citri by repressing auxin signaling in citrus (Citrus sinensis Osbeck). PLoS ONE 14(12):e0220017. https://doi.org/10.1371/journal.pone.0220017
doi: 10.1371/journal.pone.0220017
pubmed: 31830052
pmcid: 6907806